Abstract
Update
This article was updated on December 27, 2012, because of a previous error. In the Statistical Analyses of MR Imaging Examinations section and in the Table E-2 headings, the word “kappa” has been replaced with “intraclass correlation coefficient.”
Background:
Neonatal brachial plexus palsy frequently leads to glenohumeral dysplasia if neurological recovery is incomplete. Although glenoid retroversion and glenohumeral subluxation have been well characterized, humeral head deformity has not previously been quantified. Nonetheless, humeral head flattening is described as a contraindication to joint contracture release and external rotation tendon transfers. This study describes a novel technique for objectively quantifying humeral head deformity with use of magnetic resonance (MR) imaging and correlates the humeral head deformity with clinical and radiographic outcomes following joint rebalancing surgery.
Methods:
Magnetic resonance images of thirty-two children (age, 0.7 to 11.5 years) with neonatal brachial plexus palsy were retrospectively reviewed. Passive shoulder external rotation and Mallet scores were reviewed before joint rebalancing surgery and at a minimum clinical follow-up interval of two years. The humeral head skewness ratio on preoperative and postoperative axial MR images was defined as the ratio of anterior to posterior humeral head area, and this ratio was compared between affected and unaffected shoulders and with the glenoid version angle, posterior subluxation of the humeral head, and clinical parameters before and after surgery with use of paired t tests and Spearman correlation. Intraobserver and interobserver reliability of MR image measurements was determined.
Results:
Measurements of the skewness ratio on the affected side had moderate to substantial intraobserver reliability (0.53 to 0.72) and substantial interobserver reliability (0.65 to 0.71). Preoperatively, the skewness ratio of the affected humeral head (mean, 0.76; range, 0.54 to 1.03) differed significantly from the ratio in the contralateral shoulder (p < 0.05) and was significantly associated with the glenoid version angle (p < 0.05) and posterior subluxation of the humeral head (p < 0.05). Remodeling of the affected humeral head was observed postoperatively, with a significant improvement in the skewness ratio (p < 0.05). However, there were no significant correlations between the preoperative skewness ratio and postoperative clinical outcomes.
Conclusions:
Humeral head deformity in neonatal brachial plexus palsy correlated with other measures of glenohumeral dysplasia and could be reliably and objectively quantified on MR imaging with use of the skewness ratio. The humeral head deformity can remodel following joint rebalancing surgery, and such a deformity alone does not preclude a successful outcome after surgical attempts to restore glenohumeral congruity.
Level of Evidence:
Diagnostic Level IV. See Instructions for Authors for a complete description of levels of evidence.
Neonatal brachial plexus palsy affects one to three children per 1000 live births in the United States1, and it results in residual neurological deficits in 20% to 30% of affected children2. Traction injury of the brachial plexus is presumed to be related to intrauterine and extrauterine birth forces that may occur in children with macrosomia, shoulder dystocia, or assisted deliveries3. Subsequent weakness of the denervated shoulder muscles and loss of active joint motion most commonly result in an internal rotation contracture and lead to altered forces on the developing glenohumeral joint. The ensuing developmental dysplasia of the glenohumeral joint includes retroversion of the glenoid, humeral head subluxation and flattening, and ultimately humeral head dislocation4,5.
The shoulder internal rotation contractures resulting from neonatal brachial plexus palsy are commonly treated by sectioning or lengthening the subscapularis and/or pectoralis major tendons6-11. This surgery is performed with or without a concomitant transfer of the latissimus dorsi and/or teres major muscles to the posterior rotator cuff. These joint rebalancing procedures are intended to release internal rotation tightness and to augment shoulder external rotation and abduction function6-8. These surgical procedures can also lead to remodeling of the glenohumeral dysplasia, provided that the procedure is performed at a young age and an early stage of dysplasia7,9-11. The limits on patient age and dysplasia severity that preclude a successful outcome of joint rebalancing surgery are not fully defined. However, the subjective presence of humeral head flattening has been considered a contraindication to such procedures12,13. In such cases, a humeral external rotation osteotomy is generally recommended12,14,15. To date, the extent of humeral head deformity in glenohumeral dysplasia associated with neonatal brachial plexus palsy has not been objectively quantified, and the severity of humeral-sided deformity in patients undergoing joint rebalancing surgery not been correlated with clinical and imaging outcomes.
Glenohumeral dysplasia following neonatal brachial plexus palsy involves abnormalities in the shape of the glenoid and humeral head and in the relationship between the two. Existing classification schemes for glenohumeral dysplasia in neonatal brachial plexus palsy have focused on quantitative measurements of glenoid retroversion and posterior humeral head subluxation. In contrast, descriptions of humeral head flattening remain qualitative, subjective, and variable16.
The purpose of our study was threefold. First, we aimed to describe a novel method that allows for objective, quantitative, and reproducible measurement of humeral head flattening on the basis of axial magnetic resonance (MR) images of the shoulder. Subsequently, we used this method to correlate the severity of humeral head flattening before and after joint rebalancing surgery with other measures of shoulder deformity. Ultimately, we determined whether the amount of preoperative humeral head flattening correlated with postoperative functional outcome following joint rebalancing surgery.
This study was in compliance with the Health Insurance Portability and Accountability Act and was approved by our institutional review board. The requirement for informed patient consent was waived for this retrospective study.
Subjects
Thirty-two children (twenty-three girls and nine boys) with neonatal brachial plexus palsy and an internal rotation contracture treated with joint rebalancing surgery at the multidisciplinary Brachial Plexus Center at the authors’ institution were retrospectively identified. The specific indications for arthroscopic anterior release and latissimus dorsi tendon transfer, as well as the surgical technique, have been described previously7. The evaluation of humeral head deformity described in this study was not used preoperatively for surgical indications, nor was it used to guide postoperative care in these patients. The purpose of the current study was not to critically evaluate a specific surgical technique, but rather to evaluate changes in humeral head morphology following a surgical procedure that has been previously demonstrated to alter both clinical function and glenoid morphology. No other surgical procedures were performed on these patients during the study period.
Patients were included in the current study group if they had undergone preoperative and postoperative MR imaging and had undergone clinical evaluation at least two years after surgery. Preoperative MR imaging was used routinely to evaluate the degree of glenohumeral joint deformity17, and was favored over computed tomography imaging because of its superior imaging of cartilage and lack of ionizing radiation. The right side was affected in fifteen patients and the left side in seventeen. The patients ranged from 0.8 to 11.6 years of age at the time of surgery, with a median age of 2.9 years (interquartile range [IQR], 2.2 to 5.8 years). The time interval between the first and second MR imaging examinations ranged from 1.0 to 5.0 years, with a median of 1.4 years (IQR, 1.2 to 2.1 years). The time between surgery and the second MR imaging examination ranged from 11.0 to 58.7 months, with a median of 14.2 months (IQR, 12.1 to 20.4 months). The time from surgery to the latest clinical follow-up evaluation ranged from 2.0 to 5.8 years, with a median of 3.3 years (IQR, 2.3 to 4.1 years).
Clinical Assessments
Each patient underwent serial clinical assessment as a part of routine care within our institution’s multidisciplinary clinic. The preoperative measurements of passive shoulder external rotation with the arm in adduction and with the scapula stabilized were collected from a chart review, as were the Mallet shoulder function scores18.
Patients with internal rotation contractures recalcitrant to nonoperative therapy (including supervised stretching and active shoulder motion exercises) met indications for arthroscopic subscapularis release and open external rotation tendon transfers as described previously7. Patients were treated postoperatively with bracing or casting and with physiotherapy. Measurements of passive shoulder external rotation with the arm in adduction and with the scapula stabilized were made, and the Mallet scores were assessed, at the longest follow-up interval (a minimum of two years) following surgery18.
MR Imaging Examinations
All MR imaging studies were performed at the authors’ institution with use of a 1.5-T clinical system (Signa Horizon LX EchoSpeed, EXCITE HD EchoSpeed, or Signa LX EchoSpeed Plus; GE Healthcare, Waukesha, Wisconsin; or MAGNETOM Symphony 1.5T or MAGNETOM Espree 1.5T; Siemens Medical Solutions, Erlangen, Germany) or a 3-T clinical system (MAGNETOM Trio; Siemens Medical Solutions). A phased-array torso or cardiac coil was utilized to include both shoulder girdles. Both upper arms were positioned in adduction, although glenohumeral rotation was not specifically controlled. When necessary, children were sedated according to the Department of Radiology guidelines. The time between preoperative MR imaging and surgery as well as the time between surgery and postoperative MR imaging were recorded.
The shoulder MR imaging examination protocol for patients with neonatal brachial plexus palsy included at least an axial gradient-recalled echo series (300 to 400 msec TR, 6 to 13 msec TE, 20° flip angle, 256 to 384 × 192 to 384 imaging matrix, 3 to 4-mm slice, 0.5 to 1-mm gap, 1 to 2 signal averages) and an axial fast or turbo spin-echo proton-density-weighted sequence (3000 msec TR, 17 msec TE, 256 × 192 imaging matrix, 3-mm slice, 1-mm gap, 2 signal averages) that included both shoulders. An axial gradient-echo sequence with a smaller field of view of only the affected shoulder was obtained with use of the same imaging parameters as the bilateral shoulder sequence. Image matrices were similar regardless of field strength.
MR Imaging Examination Analysis
The preoperative and postoperative MR images of both the affected and the unaffected shoulder were analyzed retrospectively by the lead author (a board-certified radiologist and pediatric radiology fellow) with use of GE Centricity PACS (GE Healthcare) software. The articular surface of the humeral head was outlined on the superiormost axial gradient-recalled echo slice on which the long head of the biceps tendon was still seen within the bicipital groove. The articular surface of the humeral head was traced beginning at the medial lip of the bicipital groove, continuing medially along the humeral head articular surface, and ending posteriorly at the junction of the unossified posterior epiphysis and the ossified posterior metaphysis. This junction between hyperintense cartilage signal and hypointense bone signal is easily demarcated on gradient-echo images. A line connecting the anterior and posterior edges of the articular surface was drawn between these starting and ending points. A perpendicular bisector was then drawn medially through the line connecting the anterior and posterior margins of the articular surface, dividing the epiphysis into anterior (A) and posterior (P) regions (Fig. 1).
The area (in mm2) of the anterior region of the humeral head and the area of the posterior region were calculated by tracing the outline of the region with use of the PACS software. The anterior area was divided by the posterior area to determine the skewness ratio (SR = A/P) (Fig. 2). The term skewness ratio is used because the outline of the flattened humeral head resembles a skewed Gaussian curve (Fig. 3). Equal areas anterior and posterior to the bisection axis yield a skewness ratio of 1.
Other measures of joint deformity previously described, including the glenoid version angle and the percentage of posterior subluxation of the humeral head, were obtained according to standard techniques5. These quantities were measured on the image that showed the largest glenoid articular surface.
Statistical Analyses of MR Imaging Examinations and Clinical Assessments
All analyses were performed with use of a commercially available software program. Interobserver and intraobserver reliability were assessed with use of a randomly selected sample of 25% of the patients. The intraclass correlation coefficient (ICC) was calculated. Measurements of shoulder deformity were performed by the lead author and a senior radiologist to assess the interobserver reliability and by the lead author to assess the intraobserver reliability. By convention, an ICC value of 0.21 to 0.40 was considered to indicate fair agreement; 0.41 to 0.60, moderate; 0.61 to 0.80, substantial; and 0.81 to 1.00, almost perfect19.
The differences in morphology and function of each shoulder joint before and after surgery were examined, as were differences in a number of outcome variables between the affected and unaffected shoulders. These MR imaging variables included the skewness ratio, glenoid version angle, and posterior subluxation of the humeral head. The clinical assessment variables included the degree of passive external rotation and the total Mallet score. Comparisons for normally distributed data were made with use of the paired t test, and results are presented as the mean and the standard deviation. Comparisons for non-normally distributed data were made with use of the nonparametric Wilcoxon signed-rank test or the sign test, and results are presented as the median and the interquartile range (IQR). Differences are presented as either the mean or median difference and the corresponding 95% confidence interval (CI).
Associations between the skewness ratio (in the affected and unaffected shoulders on both the preoperative and postoperative MR imaging examinations) and the glenoid version angle, posterior subluxation of the humeral head, passive external rotation, and Mallet shoulder function score (before and after surgery) were examined with use of the paired t test and Spearman correlation (rho value). All tests were two-sided, and a p value of <0.05 was considered significant. Comparisons were specified a priori, and the reported p values were not adjusted for multiple testing.
Source of Funding
There was no external funding source for this study.
Statistical Analyses of Clinical Assessments
The mean, median, IQR, and range for imaging and clinical variable are shown in the Appendix. The median passive external rotation on the affected side was 35° (IQR, 10° to 50°) preoperatively and 80° (IQR, 63° to 90°) postoperatively. The median improvement in passive external rotation on the affected side following surgery was 40° (IQR, 0° to 63°).
The total Mallet score demonstrated an overall improvement in the function of the affected shoulder following surgery (p < 0.05). The mean total Mallet score (and standard deviation) on the affected side was 13.3 ± 2.3 preoperatively and 16.7 ± 2.3 postoperatively. The median improvement was 3.0 (95% CI, 1.0 to 5.0). Two patients were not included in the Mallet score analysis because the preoperative score was not available. One patient had a postoperative total Mallet score of 12.0, which was the same as the preoperative total score. The skewness ratio in the affected shoulder of this patient was 0.96 both before and after surgery, with no appreciable glenohumeral joint deformity on MR images. The clinical evaluations for all other patients demonstrated improvement in the total Mallet score.
Statistical Analyses of MR Imaging Examinations
The skewness ratio was obtainable from the MR imaging examinations of all children both before and after surgery. The intraclass correlation coefficients for intraobserver and interobserver reliability are shown in the Appendix. Intraobserver reliability ranged from fair to substantial for the skewness ratio on the affected side, and it ranged from moderate to almost perfect for the other imaging variables. The interobserver reliability indicated substantial agreement for all of the skewness ratio measurements except the preoperative value in the unaffected shoulder, which had moderate reliability. The interobserver reliability of the other imaging variables ranged from moderate to almost perfect.
Preoperative humeral head flattening in the affected shoulders (mean skewness ratio, 0.76 ± 0.14) was significantly greater (i.e., the skewness ratio was lower) than that in the contralateral, unaffected shoulders (0.86 ± 0.08; p < 0.05). Humeral head flattening in the affected shoulders improved significantly between the preoperative and postoperative imaging (Fig. 4), with a median improvement in the skewness ratio of 0.06 (95% CI, 0.01 to 0.14; p < 0.05). The skewness ratio on the unaffected side did not differ significantly between the preoperative and postoperative values, with a mean difference of 0.01 (95% CI, −0.03 to 0.05; p = 0.60). The difference in the skewness ratio between the affected and unaffected sides diminished to a mean of 0.02 postoperatively and was no longer significant (p = 0.36) (Table I).
The preoperative glenoid version angle ranged from −55° to 0°, with a median of −20° and an IQR of −32° to −9°. The postoperative glenoid version angle ranged from −55° to 0°, with a median of −13° and an IQR of −25° to −10°. The preoperative posterior subluxation of the humeral head ranged from 8.4% to 57.5%, with a median of 35.5% and an IQR of 24.9% to 40.4%. The postoperative posterior subluxation of the humeral head ranged from 0.2% to 56.0%, with a median of 35.4% and an IQR of 29.1% to 39.9%.
On the affected side, the preoperative skewness ratio was significantly associated with the preoperative (rho = 0.71, p < 0.05) and the postoperative glenoid version angle (rho = 0.52, p < 0.05). Likewise, the preoperative skewness ratio was significantly associated with both the preoperative (rho = 0.54, p < 0.05) and the postoperative posterior subluxation of the humeral head (rho = 0.51, p < 0.05) on the affected side. On the unaffected side, the only significant associations were between the preoperative skewness ratio and the preoperative glenoid version angle (rho = 0.41, p < 0.05), between the preoperative skewness ratio and the preoperative posterior subluxation of the humeral head (rho = 0.41, p < 0.05), and between the postoperative skewness ratio and the preoperative glenoid version angle (rho = 0.36, p < 0.05).
Following surgery, the only significant associations on the affected side were between the postoperative skewness ratio and the postoperative glenoid version angle (rho = −0.39, p < 0.05) and between the postoperative skewness angle and the postoperative posterior subluxation of the humeral head (rho = 0.41, p < 0.05).
Relationship Between MR Imaging Examinations and Clinical Assessments
Neither the preoperative nor the postoperative skewness ratio correlated significantly with preoperative or postoperative passive shoulder motion, Mallet scores, or improvements therein. The sample size provided a power of 0.80 at an alpha level of 0.05 to detect a rho of 0.46, so weaker correlations that were not detected by our study may exist.
Quantitative measures of the extent of flattening in other ball-and-socket joints have been defined previously. For example, the sphericity ratio, the lateral pillar classification, and the Stulberg classification have been used to assess the proximal aspect of femora affected with Legg-Calvé-Perthes disease20-22. Each of these classification schemes is based on conventional radiographic imaging analysis, and attempts to translate these sphericity measurements to the use of cross-sectional imaging have met with limited success23. Also, the normal humeral head has a variable “hemi-ovoid” shape rather than the more hemispherical shape of the normal femoral head, and the methods described for measuring the femoral head therefore cannot be translated easily to the humerus. Similarly, a simple measurement of the proportion of the articular surface arc of the humerus that is flat rather than round cannot be used for two reasons. First, a segment of the humeral head will subtend a smaller proportion of the arc of the articular surface as it becomes flatter, simply because a straight line is a shorter distance between two points than a curved line. Second, humeral head flattening tends to occur not as a simple loss of roundness of a particular portion of the articular surface, but rather as a global change in the humeral head shape.
Our current study suggests that obtaining an objective, quantitative measurement of axial humeral head flattening on cross-sectional MR images is feasible. In order to quantitatively measure the deformity of the humeral head, it is necessary to understand the typical pattern of flattening. In neonatal brachial plexus palsy, sufficiently severe contractures due to the denervation of upper-extremity muscles may result in posterior subluxation and internal rotation of the humerus. The resulting abnormal forces on the developing humeral head lead to flattening anteriorly and to relative “extrusion,” or asymmetrically prominent growth, posteriorly. The skewness ratio thus provides a quantitative comparison of the cross-sectional area of the flattened anterior segment of the humeral head relative to the extruded posterior segment at a reproducible cross-sectional level.
Defining specific anatomic landmarks allows for consistent measurements in each child. This quantitative assessment of humeral head deformity is consistent with existing measures of glenohumeral dysplasia following neonatal brachial plexus palsy, as indicated by the significant preoperative correlations between the skewness ratio and both the glenoid version angle and the posterior subluxation of the humeral head. It is not known how obliquity of the humeral head axial slices affects the skewness ratio, but such obliquity was minimized by placing the arm at the side, parallel to the axis of the gantry, during scanning. Such positioning minimizes the effect of a glenohumeral abduction contracture on the humeral position during scanning, although it would cause scapular rotation and thus confound glenoid morphology measurements.
Use of the skewness ratio in the current study helps to elucidate the clinical importance of humeral head deformity in these children. First, the increase in the skewness ratio postoperatively suggests that a flattened humeral head can remodel following joint rebalancing surgery, similar to the remodeling toward normal values that is observed in the glenoid version angle and the posterior subluxation of the humeral head7,9-11. Although the clinical meaning of the observed change of 0.06 in the skewness ratio of the affected side remains to be determined, the statistical significance of this improvement suggests both that the skewness ratio is sensitive to changes following surgery and that humeral head remodeling can occur. Remodeling of the humeral head would not be surprising, given the ability of largely cartilaginous structures to remodel rapidly in growing children. The significant preoperative association between the greatest degree of humeral head flattening (as determined by the skewness ratio) and the shoulders with the greatest glenoid version angle and posterior subluxation of the humeral head is also not surprising. The weaker association between the skewness ratio and measures of glenohumeral morphology on the unaffected side may be due to smaller and more random variability in these variables among normal shoulders. Second, humeral head flattening does not preclude a successful outcome after a joint rebalancing procedure, as we found no correlation between the preoperative skewness ratio and clinical outcome at a minimum of two years following surgery (assessed on the basis of improvements in passive shoulder external rotation and Mallet scores).
The lack of correlation between humeral head flattening, as measured by the skewness ratio, and clinical improvement following joint rebalancing surgery may be related to the anterior location of the flattening combined with the rounded posterior extrusion of the humeral head. Surgical release of the internal rotation contracture and augmentation of external rotation force by muscle transfers leads to a more externally rotated position of the humeral head in the glenoid. As a result, the flattened anterior portion of the humeral head is rotated out of the joint, and the rounded posterior portion is subsequently “pulled into articulation” with the glenoid. An alternative explanation for the lack of correlation between the preoperative skewness ratio and the surgical outcome is that the skewness ratio is not a robust enough measure of humeral head deformity to stratify patients for the purpose of predicting the surgical outcomes. However, the sensitivity of the skewness ratio in detecting differences in humeral head flattening among patients is supported by the correlation between the skewness ratio and other measures of glenohumeral deformity, as well as by the ability of the skewness ratio to detect postoperative changes in humeral head shape that parallel the remodeling seen in other measures of glenohumeral deformity. Regardless of the explanation, our results—based on the first reported objective, quantitative measure of humeral head deformity—refute the notion that humeral head flattening is a contraindication to joint rebalancing surgery in patients with neonatal brachial plexus palsy13.
The current study examines the relationship between the skewness ratio and clinical outcome in a subset of patients with neonatal brachial plexus palsy before and after a specific procedure. If these findings are supported by larger studies involving a wider array of patients, then the ultimate usefulness of the skewness ratio will have been to debunk the presumed clinical relevance of axial humeral head flattening in treatment decision-making. However, if larger studies are able to identify a subgroup of patients for whom the skewness ratio predicts the clinical outcome, then the measure will be clinically useful at the point of care.
The limitations of this retrospective study include a possible selection bias in the patient population, as some of our institution’s patients with brachial plexus birth palsy had indications for humeral external rotation osteotomy rather than joint rebalancing soft-tissue surgery. Nonetheless, a range of humeral head flattening was evident in our study population, and even marked flattening did not preclude a successful outcome after contracture release and tendon transfers. Another limitation is the variable times between MR imaging examinations, surgery, and clinical evaluations. Specifically, the minimum two-year follow-up interval was for clinical examinations, not for MR imaging, and an even longer time span for MR imaging follow-up could potentially allow for greater remodeling as shoulder function improves. Furthermore, given the variable timing of postoperative MR imaging, no conclusions can be drawn from this study regarding the effect of age at the time of surgery on the ability of the humeral head to remodel. Finally, we are describing a two-dimensional assessment of a three-dimensional deformity. However, currently used measures of glenoid deformity are purely two-dimensional as well, and we sought to evaluate humeral head deformity with use of the same imaging currently used for the evaluation of the dysplastic glenohumeral joint following neonatal brachial plexus palsy. It is on these two-dimensional axial images that humeral head flattening has been described qualitatively, and the present study aimed to quantify this subjective observation of deformity. The MR imaging protocol calls for the upper extremities to be placed at the patient’s side; however, the exact humeral position was not controlled in this retrospective study. Further work is needed to characterize both the glenoid and humeral sides of the dysplastic joint in three dimensions, perhaps using three-dimensional MR imaging to accomplish this aim in a clinically relevant manner in young patients with cartilaginous glenohumeral joints that are not suitable for three-dimensional computed tomography.
In conclusion, we describe the skewness ratio as a reproducible, objective, and quantitative measure of axial humeral head deformity in children with neonatal brachial plexus palsy. This measurement has a potential role in future studies in which an objective measure of the change in humeral morphology following therapy for neonatal brachial plexus palsy is desired. Furthermore, the extent of humeral head flattening did correlate with other measures of glenohumeral dysplasia preoperatively, but it did not correlate with the postoperative clinical outcome. Therefore, in contrast to prior literature suggesting that qualitative humeral head flattening indicates the need for a salvage humeral osteotomy12, we found that flattening did not prevent clinical improvement following a joint rebalancing procedure. Our findings suggest that the mere presence of humeral head flattening, in and of itself, should not preclude an attempt to restore glenohumeral congruity in this patient group.
A table summarizing the distributions of imaging and clinical variables and a table listing interobserver and intraobserver reliability are available with the online version of this article as a data supplement at jbjs.org.
Foad
SL;
Mehlman
CT;
Ying
J. The epidemiology of neonatal brachial plexus palsy in the United States. J Bone Joint Surg Am.
2008;90(
6):1258-64.[CrossRef][PubMed]
Pondaag
W;
Malessy
MJ;
van Dijk
JG;
Thomeer
RT. Natural history of obstetric brachial plexus palsy: a systematic review. Dev Med Child Neurol.
2004;46(
2):138-44.[CrossRef][PubMed]
Gilbert
WM;
Nesbitt
TS;
Danielsen
B. Associated factors in 1611 cases of brachial plexus injury. Obstet Gynecol.
1999;93(
4):536-40.[CrossRef][PubMed]
Pearl
ML;
Edgerton
BW. Glenoid deformity secondary to brachial plexus birth palsy. J Bone Joint Surg Am.
1998;80(
5):659-67.[PubMed]
Waters
PM;
Smith
GR;
Jaramillo
D. Glenohumeral deformity secondary to brachial plexus birth palsy. J Bone Joint Surg Am.
1998;80(
5):668-77.[PubMed]
Newman
CJ;
Morrison
L;
Lynch
B;
Hynes
D. Outcome of subscapularis muscle release for shoulder contracture secondary to brachial plexus palsy at birth. J Pediatr Orthop.
2006;26(
5):647-51.[CrossRef][PubMed]
Pearl
ML;
Edgerton
BW;
Kazimiroff
PA;
Burchette
RJ;
Wong
K. Arthroscopic release and latissimus dorsi transfer for shoulder internal rotation contractures and glenohumeral deformity secondary to brachial plexus birth palsy. J Bone Joint Surg Am.
2006;88(
3):564-74.[CrossRef][PubMed]
Pedowitz
DI;
Gibson
B;
Williams
GR;
Kozin
SH. Arthroscopic treatment of posterior glenohumeral joint subluxation resulting from brachial plexus birth palsy. J Shoulder Elbow Surg.
2007;16(
1):6-13. .[CrossRef][PubMed]
El-Gammal
TA;
Saleh
WR;
El-Sayed
A;
Kotb
MM;
Imam
HM;
Fathi
NA. Tendon transfer around the shoulder in obstetric brachial plexus paralysis: clinical and computed tomographic study. J Pediatr Orthop.
2006;26(
5):641-6.[CrossRef][PubMed]
Waters
PM;
Bae
DS. The early effects of tendon transfers and open capsulorrhaphy on glenohumeral deformity in brachial plexus birth palsy. Surgical technique. J Bone Joint Surg Am.
2009;91
Suppl 2:213-22.[CrossRef][PubMed]
Kozin
SH;
Boardman
MJ;
Chafetz
RS;
Williams
GR;
Hanlon
A. Arthroscopic treatment of internal rotation contracture and glenohumeral dysplasia in children with brachial plexus birth palsy. J Shoulder Elbow Surg.
2010;19(
1):102-10.[CrossRef][PubMed]
Waters
PM. Update on management of pediatric brachial plexus palsy. J Pediatr Orthop.
2005;25(
1):116-26.[PubMed]
Hui
JH;
Torode
IP. Changing glenoid version after open reduction of shoulders in children with obstetric brachial plexus palsy. J Pediatr Orthop.
2003;23(
1):109-13.[PubMed]
Waters
PM;
Bae
DS. The effect of derotational humeral osteotomy on global shoulder function in brachial plexus birth palsy. J Bone Joint Surg Am.
2006;88(
5):1035-42.[CrossRef][PubMed]
Al-Qattan
MM. Rotation osteotomy of the humerus for Erb’s palsy in children with humeral head deformity. J Hand Surg Am.
2002;27(
3):479-83.[CrossRef][PubMed]
Hogendoorn
S;
van Overvest
KL;
Watt
I;
Duijsens
AH;
Nelissen
RG. Structural changes in muscle and glenohumeral joint deformity in neonatal brachial plexus palsy. J Bone Joint Surg Am.
2010;92(
4):935-42.[CrossRef][PubMed]
Kozin
SH. Correlation between external rotation of the glenohumeral joint and deformity after brachial plexus birth palsy. J Pediatr Orthop.
2004;24(
2):189-93.[CrossRef][PubMed]
Mallet
J. [Obstetrical paralysis of the brachial plexus. II. Therapeutics. Treatment of sequelae. Priority for the treatment of the shoulder. Method for the expression of results]. Rev Chir Orthop Reparatrice Appar Mot.
1972;58:
Suppl 1:166-8. .[PubMed]
Landis
JR;
Koch
GG. The measurement of observer agreement for categorical data. Biometrics.
1977;33(
1):159-74.[CrossRef][PubMed]
Jonsater
S. Coxa plana; a histo-pathologic and arthrografic study. Acta Orthop Scand Suppl.
1953;12:5-98.[PubMed]
Stulberg
SD;
Cooperman
DR;
Wallensten
R. The natural history of Legg-Calvé-Perthes disease. J Bone Joint Surg Am.
1981;63(
7):1095-108.[PubMed]
Herring
JA;
Neustadt
JB;
Williams
JJ;
Early
JS;
Browne
RH. The lateral pillar classification of Legg-Calvé-Perthes disease. J Pediatr Orthop.
1992;12(
2):143-50.[CrossRef][PubMed]
Jaramillo
D;
Galen
TA;
Winalski
CS;
DiCanzio
J;
Zurakowski
D;
Mulkern
RV;
McDougall
PA;
Villegas-Medina
OL;
Jolesz
FA;
Kasser
JR. Legg-Calvé-Perthes disease: MR imaging evaluation during manual positioning of the hip—comparison with conventional arthrography. Radiology.
1999;212(
2):519-25.[PubMed]